Elsevier

Anaerobe

Volume 71, October 2021, 102411
Anaerobe

Review Article
Unravelling the eco-specificity and pathophysiological properties of Cutibacterium species in the light of recent taxonomic changes

https://doi.org/10.1016/j.anaerobe.2021.102411Get rights and content

Highlights

  • Genus Cutibacterium was created when genus Propionibacterium was reclassified into four genera.

  • The genus consists of five species including two new species, C. modestum and C. namnetense.

  • These species differ in their niche and pathogenicity in humans.

  • C. acnes consists of three subspecies, which also differ in their niche and pathogenicity.

Abstract

In 2016, a new species name Cutibacterium acnes was coined for the well-documented species, Propionibacterium acnes, one of the most successful and clinically important skin commensals. The nomenclatural changes were brought about through creation of the genus Cutibacterium, when a group of propionibacteria isolates from the skin were transferred from the genus Propionibacterium and placed in the phylum Actinobacteria.

Almost simultaneously, the discovery of two novel species of Cutibacterium occurred and the proposal of three subspecies of C. acnes were reported. These dramatic changes that occurred in a long-established taxon made it challenging for the non-specialist to correlate the huge volume of hitherto published work with current findings. In this review, we aim to correlate the eco-specificity and pathophysiological properties of these newly circumscribed taxa. We envisage that this information will shed light on the pathogenic potential of new isolates and enable better assessment of their clinical importance in the foreseeable future.

Currently, five species are recognized within the genus: Cutibacterium acnes, Cutibacterium avidum, Cutibacterium granulosum, Cutibacterium modestum (previously, “Propionibacterium humerusii”), and Cutibacterium namnetense. These reside in different niches reflecting their uniqueness in their genetic makeup. Their pathogenicity includes acne inflammation, sarcoidosis, progressive macular hypomelanosis, prostate cancer, and infections (bone, lumbar disc, and heart). This is also the case for the three newly described subspecies of C. acnes, which are C. acnes subspecies acnes (C. acnes type I), subspecies defendens (C. acnes type II), and subspecies elongatum (C. acnes type III). C. acnes subspecies acnes is related to inflamed acne and sarcoidosis, while subspecies defendens to prostate cancer and subspecies elongatum to progressive macular hypomelanosis. Because the current nomenclature is based upon polyphasic analyses of the biochemical and pathogenic characteristics and comparative genomics, it provides a sound basis studying the pathophysiological roles of these species.

Introduction

Cutibacterium (a cutaneous group of previously designated Propionibacterium) comprises one of the major genera of the microbiome of human skin and the eyes, and they are also well represented in the anaerobic component of human supra- and subgingival plaque and the intestinal tract [1]. The genus Cutibacterium arose out of the reclassification of genus Propionibacterium in 2016 into four genera, namely; Propionibacterium, Cutibacterium, Acidipropionibacterium, and Pseudopropionibacterium (later corrected to Arachnia), based upon habitat differences, biochemical tests and comparative genomics [2,3]. To date, five species are recognized under the genus; Cutibacterium acnes [2,4], Cutibacterium avidum [2,5], Cutibacterium granulosum [2,6], Cutibacterium namnetense [[7], [8], [9]], and Cutibacterium modestum (previously, “Propionibacterium humerusii”) [10] (Fig. 1). Since the reclassification in 2016, the new nomenclature is increasingly being used [[11], [12], [13], [14], [15], [16]]. All these species reside on the human skin as their major habitat. Previous reports indicate that C. acnes, the most predominant species of the group, is prevalent in sebaceous and dry areas of the skin, while the percentage is lower in moist areas [17]. Recently, three subspecies of Cutibacterium acnes were also established as C. acnes subspecies acnes (C. acnes type I) [[18], [19], [20]], subspecies defendens (C. acnes type II) [9,19], and subspecies elongatum (C. acnes type III) [18,20] (Fig. 1).

The taxonomy of these species and subspecies has been in a continuous state of flux (see summary, Table 1) and makes it difficult to reconcile clinical reports, which have not kept pace with changes in classification with nomenclatural changes. However, as interest in these taxa grew and new methodology was applied, taxonomic changes became inevitable. The most significant is the application of more in-depth proteomic and genomic analyses. As an example, the proposal of the subspecies of Cutibacterium acnes into Cutibacterium acnes subsp. acnes and Cutibacterium acnes subsp. elongatum were based not on traditional biochemical tests but on proteotyping methods and whole genome comparisons [18]. Because the species epithet Propionibacterium acnes has been established so long [21] whereas taxonomic changes have been so rapid and fairly recent, the old and new nomenclatures are often used interchangeably making it extremely difficult to ascertain possible correlations with specific infections. Consequently, the aim of this review is to clarify the taxonomic status of newly circumscribed taxa and draw parallels with the biology and pathogenic potential of various genotypes.

In this review, we commence with C. acnes, which is by far the best recognized species and most investigated, and then draw parallels with other Cutibacterium species to better understand the pathobiology of this group.

Section snippets

General description of the genus

Cutibacterium species are Gram positive, non-spore-forming, non-motile rods. Cells of many isolates are glass-shaped, but some isolates may be coccoid, filamentous, or V or Y-shaped [28]. Colonies on blood agar are lenticular, entire, smooth, white to light grey after 2–7 days of anaerobic culture. Growth is good under anaerobic and under microaerophilic conditions. Some isolates are aerotolerant, not only do they maintain viability under atmospheric air to grow later under anaerobic condition,

Conclusion

Phylogenetically based classification, especially whole genomes sequencing, circumscribes taxa into unambiguous taxonomic units that permit deeper insight into the biology of a species, especially its functional aspects in complex microbiomes. This is well demonstrated in the long history of the species first described as Bacillus acnes in 1891 and its later basonyms, Corynebacterium acnes and Propionibacterium acnes. Its morphological diphtheroid, coryneform rod-shaped and slightly curved

Funding source

None.

Declaration of competing interest

The authors declare that there is no conflict of interest.

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